Acoustic Aposematism and Evasive Action in Select Chemically Defended Arctiine (Lepidoptera: Erebidae) Species: Nonchalant or Not?

Abstract

Tiger moths (Erebidae: Arctiinae) have experienced intense selective pressure from echolocating, insectivorous bats for over 65 million years. One outcome has been the evolution of acoustic signals that advertise the presence of toxins sequestered from the moths’ larval host plants, i.e. acoustic aposematism. Little is known about the effectiveness of tiger moth anti-bat sounds in their natural environments. We used multiple infrared cameras to reconstruct bat-moth interactions in three-dimensional (3-D) space to examine how functional sound-producing organs called tymbals affect predation of two chemically defended tiger moth species: Pygarctia roseicapitis (Arctiini) and Cisthene martini (Lithosiini). P. roseicapitis and C. martini with intact tymbals were 1.8 and 1.6 times less likely to be captured by bats relative to those rendered silent. 3-D flight path and acoustic analyses indicated that bats actively avoided capturing sound-producing moths. Clicking behavior differed between the two tiger moth species, with P. roseicapitis responding in an earlier phase of bat attack. Evasive flight behavior in response to bat attacks was markedly different between the two tiger moth species. P. roseicapitis frequently paired evasive dives with aposematic sound production. C. martini were considerably more nonchalant and employed evasion in fewer interactions. Our results show that acoustic aposematism is effective at deterring bat predation in a natural context and that this strategy is likely to be the ancestral function of tymbal organs within the Arctiinae.

Nonchalant Flight in Tiger Moths (Erebidae: Arctiinae) Is Correlated With Unpalatability

“…However, we restricted our analysis to include only moths exhibiting "Dives" (renamed "Evasion") or "No Evasion, " as we observed "Turn Away" flight in fewer than 10% of interactions. Examples of these behaviors can be seen in Supplemental Videos 1-3 as well as Figures 6A,B from Dowdy and Conner (2016).…”

“…We define a seemingly careless demeanor in response to an immediate threat as "nonchalant." "More nonchalant" indicates slower, less complex, delayed, and/or more rarely enacted escape responses in response to a potential predatory threat (Dowdy and Conner, 2016). Because of inherent costs of fleeing, prey are expected to balance perceived predation risk with the costs of fleeing such that they initiate escape at a distance which maximizes their fitness at the end of an encounter with a predator (i.e., "Optimal Escape Model"; Ydenberg and Dill, 1986;Cooper and Frederick, 2007).…”

“…Additionally, some moths possess secondary defenses which may alter their risk of predation. Many tiger moths (Erebidae: Arctiinae) sequester defensive toxins from their host plants and produce ultrasound in response to bat echolocation, advertising their unpalatability (i.e., "acoustic aposematism"; Acharya and Fenton, 1992;Dunning et al, 1992;Hristov and Conner, 2005;Barber et al, 2009;Dowdy and Conner, 2016). Unpalatability varies between species and may relate to the concentration and type of chemical compounds they have sequestered.…”

“…Interestingly, some tiger moths have been noted to lack any significant evasive flight response to bat attacks, even though they possess and utilize ultrasonic hearing (Goldman and Henson, 1977;Acharya and Fenton, 1992;Dunning et al, 1992;Dowdy and Conner, 2016). Field experiments with certain species of tiger moths have uncovered variation in escape behaviors in response to bat attacks (Dowdy and Conner, 2016). Two sympatric tiger moth species, Pygarctia roseicapitis and Cisthene martini, differed in both the likelihood of enacting evasive dives as well as in their unpalatability.…”

Evolution of switchable aposematism: insights from individual-based simulations

“…Evolutionary biologists have explored various dimensions of aposematism, but its behavioral aspect had not received adequate attention until recent years. While some aposematic signals such as permanent coloration are fixed and operate continuously, other signals can be behaviorally controlled, by sound generation (Dowdy & Conner, 2016), wing movement (Kang et al, 2016), bioluminescence (De Cock & Matthysen, 1999), physiological color change (Umbers et al, 2014), or postural change (Lariviere & Messier, 1996). We call this form "switchable aposematism".…”